Copyright © 2013 by the author(s). Published here under license by the Resilience Alliance. Zimmerling, J. R., A. C. Pomeroy, M. V. d'Entremont, and C. M. Francis. 2013. Canadian estimate of bird mortality due to collisions and direct habitat loss associated with developments. Avian Conservation and Ecology 8(2): 10. http://dx.doi.org/10.5751/ACE-00609-080210

Research Paper, part of a Special Feature on Quantifying Human-related Mortality of Birds in Canada Canadian Estimate of Bird Mortality Due to Collisions and Direct Habitat Loss Associated with Wind Turbine Developments Estimation de la mortalité aviaire canadienne attribuable aux collisions et aux pertes directes d’habitat associées à l’éolien J. Ryan Zimmerling 1, Andrea C. Pomeroy, Marc V. d'Entremont and Charles M. Francis 1

ABSTRACT. We estimated impacts on birds from the development and operation of wind turbines in Canada considering both mortality due to collisions and loss of nesting habitat. We estimated collision mortality using data from carcass searches for 43 wind farms, incorporating correction factors for scavenger removal, searcher efficiency, and carcasses that fell beyond the area searched. On average, 8.2 ± 1.4 birds (95% C.I.) were killed per turbine per year at these sites, although the numbers at individual wind farms varied from 0 - 26.9 birds per turbine per year. Based on 2955 installed turbines (the number installed in Canada by December 2011), an estimated 23,300 birds (95% C.I. 20,000 - 28,300) would be killed from collisions with turbines each year. We estimated direct habitat loss based on data from 32 wind farms in Canada. On average, total habitat loss per turbine was 1.23 ha, which corresponds to an estimated total habitat loss due to wind farms nationwide of 3635 ha. Based on published estimates of nest density, this could represent habitat for ~5700 nests of all species. Assuming nearby habitats are saturated, and 2 adults displaced per nest site, effects of direct habitat loss are less than that of direct mortality. Installed wind capacity is growing rapidly, and is predicted to increase more than 10-fold over the next 10-15 years, which could lead to direct mortality of approximately 233,000 birds / year, and displacement of 57,000 pairs. Despite concerns about the impacts of biased correction factors on the accuracy of mortality estimates, these values are likely much lower than those from collisions with some other anthropogenic sources such as windows, vehicles, or towers, or habitat loss due to many other forms of development. Species composition data suggest that < 0.2% of the population of any species is currently affected by mortality or displacement from wind turbine development. Therefore, population level impacts are unlikely, provided that highly sensitive or rare habitats, as well as concentration areas for species at risk, are avoided. RÉSUMÉ. Nous avons évalué les impacts de la construction et de l’opération de parcs éoliens sur les oiseaux au Canada en considérant la mortalité attribuable tant aux collisions qu’à la perte d’habitat de nidification. Nous avons estimé la mortalité par collision à partir de données provenant de la recherche de carcasses dans 43 parcs éoliens, et avons inclus des facteurs de correction tenant compte de l’efficacité des observateurs, de la persistance des carcasses et du fait qu’elles pouvaient se trouver à l’extérieur de l’aire couverte par les recherches. En moyenne, 8,2 ± 1,4 oiseaux (IC à 95 %) ont été tués par éolienne par année dans ces parcs, quoique ce nombre a varié de 0 à 26,9 oiseaux par éolienne par année lorsque les parcs ont été pris individuellement. Fondé sur 2 955 éoliennes construites (bilan en décembre 2011 au Canada), nous estimons que 23 300 oiseaux (IC à 95 % = 20 000 à 28 300) seraient tués à la suite de collisions avec les éoliennes chaque année. Nous avons ensuite estimé la perte directe d’habitat à partir de données de 32 parcs éoliens au Canada. En moyenne, la perte d’habitat par turbine s’élevait à 1,23 ha, ce qui équivaut à 3 635 ha d’habitat perdu au profit d’éoliennes dans l’ensemble du Canada. Selon des estimations de densité de nids publiées, une quantité d’habitat de cet ordre pourrait contenir 5 700 nids, toutes espèces confondues. En présumant que les milieux voisins sont saturés et que deux adultes sont déplacés par site de nidification, les effets de la perte d’habitat directe sont moins importants que ceux qui sont attribuables à la mortalité directe. Or, la puissance éolienne installée augmente rapidement et on prévoit qu’elle se multipliera par plus de dix d’ici 10 à 15 ans, ce qui pourrait se traduire par la mortalité directe d’environ 233 000 oiseaux/année et le déplacement de 57 000 couples. Malgré les préoccupations quant aux impacts des biais des facteurs de correction sur la précision des estimations de la mortalité, ces valeurs sont vraisemblablement moins élevées que celles calculées pour les collisions avec d’autres sources anthropiques comme les fenêtres, les véhicules ou les tours, ou encore celles associées à la perte d’habitat attribuable à de nombreuses autres formes de développement. Les données sur la composition spécifique indiquent que < 0,2 % des populations, peu importe l’espèce, est en réalité touchée par la mortalité ou le déplacement

1Canadian Wildlife Service Avian Conservation and Ecology 8(2): 10 http://www.ace-eco.org/vol8/iss2/art10/

occasionné par le développement éolien. Ainsi, les répercussions sur le plan des populations sont peu probables, pourvu que les milieux très sensibles ou rares, de même que les aires de concentration d’espèces en péril soient évités. Key Words: bird populations; Canada; collision mortality; correction factors; habitat loss; wind turbine

INTRODUCTION large-scale wind energy facilities in California, e.g., Altamont Although is widely viewed as a clean alternative (Orloff and Flannery 1992). Although some reports suggest to -based energy generation, there has been some that newer wind facilities are generally associated with lower concern regarding the impact of wind farms on birds (Kern bird fatality rates (Erickson et al. 2001, 2005), others propose and Kerlinger 2003, Langston and Pullan 2003, Kingsley and that the more modern turbine designs, with taller towers and Whittam 2005, Drewitt and Langston 2006, Barclay et al. larger blade lengths with higher tip speeds, pose higher 2007, Smallwood 2013). Birds can be killed through collisions collision risks (Morrison 2006). For nocturnal migrants, there with turbines and other ancillary structures such as is little evidence that particular species of birds are more meteorological (met) towers or power lines, and through nest vulnerable than others, and mortality is thought to be mortality if vegetation clearing, required for project proportional to the relative abundance of each species (Drewitt development, occurs during the nesting season (Band et al. and Langston 2006). Current levels of mortality are not 2007, Smallwood and Thelander 2008). Construction thought to impact most individual bird populations (Kuvlesky associated with wind turbines can also lead to loss of nesting et al. 2007, Arnold and Zink 2011). Nevertheless, these habitat, thus reducing the carrying capacity or productivity of collisions contribute to the cumulative mortality of birds a site in the longer term. (Gauthreaux and Besler 2003) and potentially could influence the long-term viability of some populations. Particular concern Most turbine collision studies have reported low levels of has been expressed that even low levels of mortality for species overall bird mortality (Drewitt and Langston 2006, 2008), with low population densities and slow reproductive rates, especially when compared to mortality from other man-made such as raptors, could have population level impacts (Manville structures such as communication towers (Kerlinger et al. 2009). 2011, Longcore et al. 2012). Results from mortality studies at various sites in the United States and Europe generally suggest Nest mortality and the displacement of breeding pairs through that annual bird collisions range from 0 to over 30 collisions loss of habitat may also occur when habitat is removed for the per turbine, although data collection protocols, experimental construction of turbine pads, access roads, and power lines design, and analysis methods varied substantially among wind (Pearce-Higgins et al. 2012). Such impacts are similar to those farms, making many studies difficult to compare (Kuvlesky from many other types of development, but nevertheless et al. 2007, Sterner et al. 2007, Stewart et al. 2007, Ferrer et represent a potential impact of a . Newer facilities al. 2012). Erickson et al. (2001) estimated 33,000 birds killed are constructed with larger, more efficient turbines that result per year based on 15,000 turbines in the United States for an in fewer turbine pads and roads per unit of energy. In Canada, average of 2.1 birds/turbine/year. Manville (2009) suggested most wind farms have been built in agricultural areas or other that this may be a considerable underestimate, and provided disturbed areas, but some have been built in areas that were a number of 440,000 birds per year with 23,000 turbines formerly relatively undeveloped, e.g., contiguous forest. installed, but did not provide a rationale for the revised Wind energy development in Canada has grown dramatically number. Smallwood (2013) estimated 11.1 birds/megawatt/ in recent years and has been subject to considerable effort for year (or 22.2 birds per turbine for a typical modern 2 MW environmental assessment, relative to many other forms of turbine), which would represent about 573,000 birds killed development, but a comprehensive analysis of data from each year across an installed capacity in 2012 of 51,630 Canadian sites has not yet been undertaken (Smallwood [2013] megawatts. One report from Spain (Atienza et al. 2011) used data from only two Canadian sites). Installed capacity of suggested mortality rates could be as high as 300 - 1000 birds/ commercial wind power in Canada increased by 750% turbine/year, but little justification was provided for this between 2005 and 2011; as of December 2011, there were over estimate. 135 wind farms with 2955 wind turbines in the country, and Passerines typically comprise 80% of all fatalities, most of this number is expected to increase tenfold over the next 10 - which involve nocturnal migrants (Mabee et al. 2006, 15 years (CANWEA 2011). The high effort required for Kuvlesky et al. 2007), but some of the greatest concern has environmental assessments has been due partly to uncertainty related to raptors. The behavior of some diurnal migrating about the impacts of a relatively new and changing technology, birds, such as raptors, makes them vulnerable to collisions as well as concerns about wildlife impacts observed at some with wind turbines, particularly if they are hunting (Higgins of the early facilities such as those in California. As a result, et al. 2007, Garvin et al. 2011, Martínez-Abraín et al. 2012). many facilities have undergone lengthy baseline studies for Raptor mortality rates were particularly high at some early, multiple seasons and years to determine wildlife use of the site Avian Conservation and Ecology 8(2): 10 http://www.ace-eco.org/vol8/iss2/art10/

(Stantec, unpublished report; Jacques Whitford Ltd., of carcasses retrieved may vary among study. Nevertheless, unpublished report). The results of these studies have, at some by taking into account appropriate correction factors specific sites, influenced the location of turbine locations within a wind to the methodology in each study, it is possible to estimate facility (Golder Associates Ltd., unpublished report) and, mortality rates, and make direct comparisons among studies. occasionally, influenced the decision whether or not to We estimated collision mortality based on data collected from proceed with development of a wind facility (e.g., National searching for carcasses around a fixed distance, usually 50 m, Wind Watch 2011). Once constructed, many sites have carried from the base of turbines, and corrected for incomplete out extensive postconstruction studies to monitor direct detection. Carcass searches are only expected to find some of mortality caused by wind turbines to birds and other wildlife. the birds killed by turbines. Some carcasses may be removed

by scavengers, others may land outside the search area, while We analyze available data on bird mortality from others may be overlooked by the searcher. Each of these factors postconstruction monitoring reports in Canada to derive may vary among studies depending upon the terrain, the area national and provincial estimates of total bird mortality from searched, and the individual searching in the field. We applied collisions with wind turbines, and compare them with a standardized approach to correcting the raw data using published estimates from other countries and estimates of bird Equation 1, which is similar to that used for postconstruction mortality from other forms of development. We also estimate monitoring studies in some provinces (e.g., OMNR 2011): the loss of breeding habitat, and potential rates of nest mortality C = c / (Se * Sc * Ps * Pr * Py) (1) as a result of construction activities. Although we acknowledge that other wildlife, particularly bats, may also where, C = corrected number of bird mortalities, c = number be impacted by wind power projects, we limited our current of carcasses found, Se = proportion of carcasses expected to analyses to impacts on birds. be found by searchers (searcher efficiency), Sc = proportion of carcasses not removed by scavengers over the search period METHODS (scavenger removal), Ps = proportion of area searched within Collision mortality data a 50 m radius of turbines (assuming a uniform distribution of We obtained all available postconstruction monitoring reports carcasses within the 50 m radius), Pr = proportion of carcasses for sites across Canada that had been submitted to Natural expected to fall within the search radius, and Py = proportion Resources Canada as part of the postconstruction monitoring of carcasses expected during the times of year that surveys requirements of an environmental assessment. We also took place. Our analyses assumed that all carcasses found were obtained data from postconstruction monitoring reports killed as a result of collisions with turbines. published on wind developers’ or their consultants’ websites, All but three of the studies we analyzed estimated both as well as some confidential data directly from developers or searcher efficiency and scavenging rates specific to their study their consultants on the condition that they could be used for design and study area. There was substantial variation in the this analysis, but could not be publically released. These estimated values for searcher efficiency (range 0.30 to 0.85) reports provide the results of carcass searches conducted at and scavenger removal rates (range 0.10 to 0.91) highlighting the base of turbines at operating wind farms; however, few the importance of using site-specific values whenever include mortality data from meteorological towers or above possible. Differences in searcher efficiency are expected ground power lines so those were excluded from our study. because of variation in the habitat being searched, which We obtained data for wind farms in eight provinces, but were varied from gravel pads to agricultural fields to regenerating unable to obtain relevant data for wind farms in the Yukon, vegetation, as well as differences in observers and their Manitoba, or Newfoundland and Labrador. There are currently experience. Scavenger rates are also expected to vary among no wind farms operating in the Northwest Territories or sites, depending both on the habitat, which affects the ease Nunavut. with which scavengers can find carcasses, as well as the Most data in postconstruction monitoring reports were scavenger community in any given area, which potentially collected by environmental consultants contracted by the wind includes birds, mammals, and invertebrates such as ants and energy developer. Data collection methodologies used to burying beetles (Labrosse 2008). estimate mortality were not standardized and therefore varied We acknowledge the possibility that some estimates of somewhat between wind energy developments and detection probabilities and scavenger removal rates may be consultants, especially prior to 2007 when federal biased in various ways. In some studies, multiple observers environmental assessment guidelines for birds were published with different levels of experience may have carried out the (Environment Canada 2007a,b). The lack of standardization carcass searchers, but only a single value of searcher efficiency in data collection protocols means that the raw carcass counts was provided, and it was not clear whether this was an may not be comparable among studies because the proportion appropriately weighted average across observers. Some Avian Conservation and Ecology 8(2): 10 http://www.ace-eco.org/vol8/iss2/art10/

reports indicated that carcasses used for searcher efficiency transects to provide uniform coverage through the search area. and or scavenger trials were not always placed in the same In three studies, a 120 x 120 m square grid was searched around habitat types where carcass searches were conducted; if they each turbine, while one used a 160 x 160 m square grid. All were concentrated in habitats that were easier or harder to of these studies provided complete coverage out to 60 m, but search, this could have created a bias. The type of carcasses to estimate the number of carcasses that fell between 60 - 85 used in the searcher efficiency and scavenger removal trials m from the turbine, we extrapolated the number of carcasses also varied among projects: most studies used migratory birds found per square meter in the corners of the square search grid that had previously been found around turbines, but a few used to a circle with a radius of 85 m. Averaged across these four young chickens and quail of varying ages. Labrosse (2008) studies, we estimated that only 48.2% of carcasses fell within demonstrated that detection probability associated with a 50 m radius. This estimate is very close to an estimate based carcasses increases with the contrast and color against the on our own unpublished study in spring 2013 that searched background. If domesticated birds are used for searcher the entire 85 m radius around turbines in an agricultural area efficiency trials, this could lead to biased estimates if they are and found 58 carcasses of which only 46.5% were within a 50 more conspicuous than typical wild birds. Furthermore, m radius. We applied a correction factor of 48% (a weighted searcher efficiency trials should be done “blind” so that the average of these studies) to the estimated mortality for all wind searcher is unaware when they are being tested to avoid farms that only searched up to a 50 m radius. changes in search patterns on testing days, but if the searcher Most sites were only surveyed for part of the year, generally finds a domestic bird he/she will immediately be aware of the in seasons when the highest risk of mortality was anticipated, trial. Scavenger removal trials may also have been biased if usually the spring and autumn migration periods. In one case, they were only carried out during part of the season, if domestic only three months, i.e., one season, of postconstruction birds instead of wild birds were used, if they were not placed monitoring data were collected. Most of the reports provided in all of the habitats being searched, or if some of the carcasses the total number of carcasses and estimated total mortality per had already been dead for a while; freshly dead birds are likely site only for seasons that were surveyed. To extrapolate to be scavenged much faster than birds that have been dead estimates to an annual total (Py), we used data from four wind for several days and are partly dehydrated (Van Pelt and Piatt farms in and one in that were surveyed for up 1995). For the purpose of this study, we have accepted the to two years throughout the annual cycle, and for which values provided in the individual studies, but recognize that, mortalities were reported for each month. Using these data, in some cases, this may lead to bias, an issue which we consider we estimated the monthly distribution of mortality throughout in the discussion. the year. We then estimated annual mortality for other sites Most studies did not estimate the proportion of birds expected by dividing the corrected number of bird mortalities per turbine to fall beyond the typical 50 m search radius (Pr), so we used by the proportion of mortalities expected during the actual standardized estimates based on a limited number of studies dates that surveys took place, e.g., in Alberta, on average, 95% that monitored a larger search area. The distribution of of mortalities occurred between April and November; in carcasses in relation to distance from the turbines is unlikely Ontario, 98.5% of mortalities occurred during this time period. to vary much among sites, because it is affected mainly by the For sites in Ontario and east, we used the Ontario estimate, height of the turbines (Hull and Muir 2010), which is very whereas for sites in Manitoba and west we used the Alberta similar for most Canadian turbines, and is not affected by estimate of proportion of mortalities expected during the actual habitat, searcher efficiency, or scavengers. Hull and Muir dates that the surveys took place. We acknowledge that there (2010) used a Monte-Carlo approach based on ballistics to are limitations to extrapolating results from one season to other model the proportion of carcasses that would be thrown seasons based on only five studies, because seasonal patterns various distances from a turbine, assuming that birds acquire of mortality rates may vary among locations. However, a forward momentum based on the speed of the blade and are because most studies concentrated their efforts during seasons equally likely to be hit anywhere along the length of the blade. with the highest expected mortality, and because relatively For turbines with an 80 m high and 45 m long blades, few birds are found during the summer and winter months, similar to most Canadian turbines, they suggested that 99% of any error associated with extrapolation to these seasons is small birds (10 g) would land within 71 m of the turbine base. unlikely to have much impact on our estimates. This distance increases to nearly 90 m for midsized birds (680 We applied the appropriate correction factors (Equation 1) to g), and 115 m for large birds (4500 g). Because most birds all 43 wind farms using the data provided in reports on searcher killed at Canadian turbines were small to midsized, we efficiency, scavenger rates, and area searched. Where multiple assumed that a radius of 85 m would include nearly all years of data were collected at a site, we used the average of individuals, and used empirical data from postconstruction all years for the analysis. In some studies, there were monitoring reports that had searched areas up to 85 m around insufficient data to apply correction factors and estimate turbines in open habitats. All of these studies used equal-width mortality for each season, i.e., spring and fall, so we used Avian Conservation and Ecology 8(2): 10 http://www.ace-eco.org/vol8/iss2/art10/

average factors. At one wind farm in Alberta, searcher StatusReport2012_final.pdf) to obtain estimates of the total efficiency was not reported and, at two wind farms, scavenger population size of each of the 10 most abundant species in impacts were not reported. In these cases, we applied the carcass searches as well as any species listed as Endangered average values for wind farms in Alberta (Se = 0.65 and Sc = or Threatened under the Species At Risk Act (Government of 0.61). We did not include data from any reports in our analysis Canada 2002). Population impact for each species was then where both searcher efficiency and scavenger impact data calculated as the total estimated mortality for that species were absent, or where surveys occurred for less than three divided by its estimated population size. months throughout the year. Loss of nesting habitat To determine if there was any significant variation in estimated We used information from 32 environmental assessments and mortality among provinces, we conducted a one-way Analysis postconstruction reports for wind energy developments in of Variance (ANOVA) using estimated average mortality for Canada to estimate total habitat loss from power lines, roads, each of the 43 wind farms as the sampling unit and province substations, laydown areas, and turbine pads at each site. There as the predictor variable. We estimated avian mortality for is some evidence that habitat loss increases in an each province based on estimated average mortality per approximately linear fashion with wind farm size, e.g., number turbine in that province for studies for which we had data, of turbines (Stantec, unpublished report). As such, we summed multiplied by the total number of turbines in the province. For habitat loss from each component and presented the value as provinces without any collision data, we used the estimated habitat loss (ha) per turbine. Average habitat loss per turbine averaged mortality per turbine across Canada. We estimated per wind farm was calculated and extrapolated to predict total collision mortality for wind farms across Canada as the habitat loss per turbine at the remaining 103 wind farms. sum of the provincial estimates. We used ecological land classification, habitat mapping or We did not analyze whether specific turbine model types or remote-sensing imagery provided in the environmental characteristics posed a higher risk to birds relative to other assessments to classify habitats for the 32 wind farms as types because there was relatively little variation in the total agriculture, grasslands, deciduous forest, coniferous forest, or height of wind turbines (hub height plus rotor radius) in the mixed forest. Habitat data provided in many environmental sample for which we had data. Of the wind farms analyzed in assessments were insufficient to provide finer-scale this study, 81% started their postconstruction monitoring classifications. The remaining 103 wind farms for which studies after 2007, and based on a review of turbine environmental assessments could not be obtained were located specifications, we found that the total height (tower and based on their geographical coordinates, and assigned to one blades) of nearly all of the turbines erected since 2007 was of these broad habitat classifications based on SPOT satellite between 117 m and 136 m with a nameplate capacity of 1.5 imagery for the location. Nest densities in these habitats were MW to 3.0 MW. estimated based on previous Canadian studies of incidental take due to forestry operations (Hobson et al. 2013), mowing, Species-specific population impacts and other mechanical operations in agricultural landscapes We estimated the population relevance of mortality as the (Tews et al. 2013). We used the MODIS land cover number of individuals of each species lost from collisions per classification layer to calculate the total area of each broad year with wind turbines relative to the total estimated habitat type and province and the Hobson et al. (2013) and population size of that species. Of the 43 reports reviewed, 37 Tews et al. (2013) nest densities to estimate total number of reported species composition of the fatalities. Because nests. The percent of nesting habitat lost for a given habitat relatively few individuals of any one species were detected at type in a province was calculated by dividing the predicted each site, we pooled species-composition data across all sites habitat lost from wind energy developments by the total area to estimate the percentage of mortalities that were represented for that habitat type across the province. by each species. The annual mortality estimate of each species at a national scale was calculated using Equation 2: RESULTS Mortality Species X = Mortality/turbine * # Turbines * % Collision mortality estimates carcasses Species X (2) Estimates of collision mortality among the 43 wind farms We used the Partners in Flight (PIF) landbird population varied between 0 and 26.9 birds per turbine per year. On database (http://rmbo.org/pif_db/laped/), Status of Birds in average, estimated mortality (± 95% C.I.) was 8.2 ± 1.4 birds Canada (http://www.ec.gc.ca/soc-sbc/index-eng.aspx?sL= per turbine per year. There was no significant variation in e&sY=2010), and the USFWS Waterfowl Population Status estimated mortality per turbine among provinces in Canada

2012 report (http://www.fws.gov/migratorybirds/ (F7,35 = 1.52, p = 0.191). Based on 2955 installed turbines (the NewReportsPublications/ PopulationStatus/Waterfowl/ number installed by December 2011), the estimated annual Avian Conservation and Ecology 8(2): 10 http://www.ace-eco.org/vol8/iss2/art10/

Table 1. Estimated bird mortality per turbine from collisions at wind farms with available carcass search data, and estimated total mortality per province based on the number of installed turbines.

Province/Territory No. of No. of Turbines No. of Wind Farms Estimated Mortality/ Predicted Estimated Wind Farms Analyzed Turbine Mortality Yukon (YK) 2 2 0 8.2† 16 British Columbia (BC) 3 83 2 8.4 697 Alberta (AB) 26 588 7 4.5 2646 Saskatchewan (SK) 5 132 3 10.1 1333 Manitoba (MB) 3 123 0 8.2† 1009 Ontario (ON) 38 965 19 10.8 10,422 (QC) 15 672 2 5.2 3494 New Brunswick (NB) 4 113 2 2.4 271 Nova Scotia (NS) 26 161 6 11.2 1803 Prince Edward Island (PE) 9 90 2 15.2 1368 Newfoundland (NF) 4 26 0 8.2† 213 Total 135 2955 43 23,273 †Where no data were available for a particular province, the weighted national estimate was used. mortality across Canada was 23,300 birds (95% C.I. 20,000 - derived from reports from individual studies in Canada. This 28,300). Nearly half of all collisions occurred in the province is due mainly to incorporation of two additional correction of Ontario where the highest numbers of turbines are installed factors: the proportion of birds likely to fall outside a 50 m (Table 1). search radius, and the proportion of birds killed at other times of year. Nevertheless, our estimates are lower than some recent Species-specific population impacts estimates for bird mortality in the United States. Manville Overall, the 37 reports that recorded species composition (2009) suggested that annual bird mortality from wind power during postconstruction mortality surveys identified 1297 bird projects in the United States was 440,000 birds, which equals carcasses of 140 species. The most frequently recovered about 19 birds per turbine based on an estimated 23,000 species were Horned Lark (Eremophila alpestris), Golden- turbines at the time. However, he did not provide any details crowned Kinglet (Regulus satrapa), Red-eyed Vireo (Vireo on how this estimate was derived. Smallwood (2013) olivaceus), European Starling (Sturnus vulgaris), and Tree undertook a detailed assessment of correction factors based Swallow (Tachycineta bicolor; Table 2). For the most on data from 60 different reports, and estimated an average commonly recovered carcasses, and also for species at risk, mortality of 11 birds per MW per year, implying 22 birds per collision mortality was estimated to have an annual impact of turbine for a 2 MW turbine. Extrapolated to an installed less than 0.8% of any population at a national level (Table 2). capacity of 51,630 MW in the United States, this implies Loss of nesting habitat and nest mortality estimates 573,000 bird fatalities per year. Most of the difference in On average, total habitat loss per turbine at 32 wind farms in Smallwood’s estimates, compared to ours, appears to be due Canada was 1.23 ± 0.72 ha. Based on this average, the to differences in the correction factors rather than a difference predicted total habitat loss for wind farms nationwide was in the number of carcasses found in the data he analyzed. For 3635 ha (Table 3). Using the nest density estimates provided example, he used larger corrections for birds falling outside a in Hobson et al. (2013) and Tews et al. (2013), the total number 50 m radius; by assuming a logistic distribution of carcasses, of potentially affected nests in each habitat for all represented he concluded that carcasses could fall up to 156 m away from provinces was 5715. We had few data on the timing of an 80 m turbine, though this is farther than Hull and Muir construction activities to estimate the number of nests that (2010) suggested is likely. Furthermore, his analysis assumes might have been disturbed or destroyed during construction. that mortality is proportional to the rated capacity of the The amount of nesting habitat disturbed or destroyed was turbines, but particularly for newer turbines this seems estimated to vary from 0.002% of coniferous forest in the unlikely; for example, there is only a 19% increase in the blade Yukon Territory to almost 8% of mixed forest in Prince swept area between a 1.5 and 3.0 MW turbine (http://site.ge- Edward Island (Table 3). energy.com/prod_serv/products/wind_turbines/en/15mw/specs. htm; http://www.vestas.com/en/wind-power-plants/procurement/ DISCUSSION turbine-overview/v90-3.0-mw.aspx#/-univers). A report from Spain estimated that annual mortality was between 300 - Collision mortality estimates 1000 birds per turbine (Atienza et al. 2011), but examination Our estimates for average annual mortality per turbine at wind of the underlying data suggests similar number of carcasses farms in Canada of 8.2 birds is higher than most estimates were found in Spain as in Canada. Their very high mortality Avian Conservation and Ecology 8(2): 10 http://www.ace-eco.org/vol8/iss2/art10/

Table 2. Reported mortality and estimated annual collision mortality and percent of Canadian population impacted for the 10 species most frequently reported as casualties, as well as two species at risk.

Species No. of Carcasses Proportion of Total Total Predicted Canadian Population % of Population Mortality† Estimate‡ Horned Lark 135 0.10 2327 30,000,000 0.008 (Eremophila alpestris) Golden-crowned Kinglet 92 0.07 1629 23,000,000 0.007 (Regulus satrapa) Red-eyed Vireo 80 0.06 1396 96,000,000 0.001 (Vireo olivaceus) European Starling 66 0.05 1164 30,000,000 0.004 (Sturnus vulgaris) Tree Swallow 53 0.04 931 12,000,000 0.008 (Tachycineta bicolor) Red-tailed Hawk 40 0.03 698 582,000 0.120 (Buteo jamaicensis) Ring-billed Gull 27 0.02 465 1,000,000 0.047 (Larus delawarensis) Mourning Dove 26 0.02 465 5,300,000 0.009 (Zenaida macroura) Mallard 20 0.02 465 7,200,000 0.006 (Anas platyrhynchos) Purple Martin 20 0.02 465 523,000 0.089 (Progne subis) Canada Warbler 4 0.003 70 1,350,000 0.005 (Cardellina canadensis; THR)§ Chimney Swift 4 0.003 70 145,000 0.048 (Chaetura pelagica; THR)§ † Extrapolation based on 2955 turbines across Canada, and assuming that species composition of sampled sites is representative of all sites, ignoring variation in habitat and species distributions. ‡ Based on estimates from various sources (see Methods). § Threatened on Schedule 1 of Species At Risk Act.

estimates were based on assumptions that searcher efficiency other structures in the landscape. For example, in the United was extremely low, scavenger rates were very high, and large States, there were an estimated 100 million residential numbers of carcasses fell outside the search areas. However, buildings and average mortality is estimated to be five birds no evidence was presented to support those assumptions, and per building (see Klem 1990). However, mortality per it is quite possible that mortality rates were not actually any structure is also higher for many other structures than wind higher than those in Canada. turbines. For example, in Canada, the average annual mortality rate from communication towers is estimated to be 28 birds We estimated total mortality across all sites in Canada at about per tower (Longcore et al. 2012) compared to 8.2 birds per 23,300 birds per year based on 2955 turbines. Installed wind wind turbine. Several studies have suggested that many capacity is growing rapidly in Canada, and is predicted to migratory birds exhibit avoidance behavior when approaching increase more than tenfold over the next 10 - 15 years, which modern wind turbines (e.g., Erickson et al. 2002, Zdawczyk could lead to direct mortality of approximately 233,000 birds 2012), which may partly explain relatively low mortality per year. Based on Smallwood’s (2013) analysis, current compared to other structures. mortality in the United States is estimated at 573,000 birds per year which, with a projected sixfold increase over the same We found substantial variation among sites in the estimated time period could lead to direct mortality of over 3 million mortality per turbine, ranging from 0 to 27 birds per year, but birds per year. Even at these levels, estimated mortality little variation among provinces, although for several associated with wind turbines would still be lower than those provinces we only had data from a few sites. Some natural from some other anthropogenic sources. Erickson et al. (2005) variation in mortality estimates is expected because of site- estimated 500 million birds killed annually due to collisions specific characteristics that may concentrate migratory birds with residential buildings, 130 million for collision with power in some areas and not in others. For example, landscape lines, 80 million for collisions with vehicles, and 100 million features such as promontories and large bodies of water are due to domestic and feral cats. To some degree, these more likely to concentrate migratory birds along the shoreline differences in impacts are due to the much larger numbers of (e.g., Diehl et al. 2003), as are largely forested landscapes Avian Conservation and Ecology 8(2): 10 http://www.ace-eco.org/vol8/iss2/art10/

Table 3. Estimated habitat loss, number of nests lost, or breeding pairs displaced, and percent of nesting habitat lost for each habitat by province.

Province Habitat No. of No. of Predicted Nests/ha Estimated No. of Area of habitat (ha) % of nesting wind Turbines habitat nests lost/pairs habitat lost farms loss (ha) displaced Yukon Coniferous Forest 2 2 2.5 4 10 123,200 0.002 British Columbia Mixed Forest 3 83 102.1 5 510 132,000 0.077 Alberta Agriculture 21 532 654.4 0.2 131 88,700 0.737 Alberta Grassland 5 56 68.9 0.8 55 75,300 0.092 Saskatchewan Agriculture 5 132 162.4 0.2 32 122,800 0.132 Manitoba Agriculture 3 123 151.3 0.2 30 30,600 0.494 Ontario Agriculture 32 875 1076.3 0.2 215 32,300 3.33 Ontario Deciduous Forest 2 86 105.8 7.8 825 110,000 0.096 Ontario Urban 4 4 4.9 0.2 1 2700 0.183 Quebec Agriculture 10 506 622.4 0.2 124 20,800 2.99 Quebec Mixed Forest 5 166 204.2 6.2 1266 247,900 0.082 New Brunswick Coniferous Forest 1 33 40.6 7.2 292 4600 0.891 New Brunswick Mixed Forest 3 80 98.4 6 590 25,400 0.386 Nova Scotia Mixed Forest 25 127 156.2 6.2 969 16,500 0.945 Nova Scotia Deciduous Forest 1 34 41.8 5.7 238 25,400 0.165 Prince Edward Island Agriculture 4 62 76.3 0.2 15 2300 3.36 Prince Edward Island Mixed Forest 5 28 34.4 6.2 214 430 7.96 Newfoundland Mixed Forest 4 26 32.0 6.2 198 59,000 0.054 TOTAL 135 2955 3635 5715 relative to predominately agricultural landscapes (Buchanan correction factors may also be biased low if some birds fall 2008). Based on data from the postconstruction monitoring beyond 85 m (Jain et al. 2007, 2009, Smallwood 2013), reports, we were unable to identify factors other than although ballistic modeling suggests very few birds are correction factors that may explain variation in mortality expected beyond that distance (Hull and Muir 2010). On the among sites. other hand, we assumed that all birds found during carcass searches died as a result of colliding with the turbines. If some The accuracy of collision mortality estimates depends both on of these birds died from other sources of mortality unrelated the quality of the carcass search data, and the accuracy of to wind turbines (e.g., see Nicholson et al. 2005), this would correction factors used to account for incomplete carcass lead to an overestimate of the impacts of turbines. detections. If search effort is only sufficient to detect a few (or no) carcasses, estimates will be unreliable regardless of The net effect of these various potential biases, both positive correction factors. Potential biases in correction factors could and negative, is difficult to predict, because some may cancel lead to either over or under estimates of mortality. Several each other, but overall we believe that our estimates are factors could lead to overestimates of searcher efficiency, probably reasonable. Furthermore, we note that, despite some including use of inappropriate carcasses that may be more potential biases, the wind industry has some of the most conspicuous or larger than species that would be expected to reliable data for estimating incidental mortality to birds of any be found during carcass searches (Labrosse 2008), industrial sector in Canada. Even if we have underestimated concentrating carcasses in more exposed habitats within the some of the correction factors, and the actual mortality is search area, and failing to ensure that searcher efficiency trials double what has been reported, it is still low compared to other occur without the knowledge of the observer. Scavenger rates industrial sectors. may be biased if carcasses used in the trials are not fresh (Smallwood 2013), are not representative of the species being Species-specific population impacts detected, or if too many carcasses are used at one time for The short-term population effects of wind power in Canada trials, i.e., scavenger swamping (Smallwood et al. 2010). All on most species appear to be relatively negligible. Generally, of these could result in underestimates of mortality. On the the birds recorded in carcass searches were abundant species other hand, many studies estimate scavenger removal over the with large populations. For example, Horned Lark, Golden- total search interval, e.g., three days. This may lead to an crowned Kinglet, Red-eyed Vireo, European Starling, and overestimate because, on average, one would expect carcasses Tree Swallow were the most commonly impacted species. For to be exposed to potential scavengers for only half the search the five most common bird species, the effect of collisions period, e.g., for a typical three-day search interval, birds would with wind turbines is unlikely to affect their conservation be equally likely to be killed one, two, or three days before because the estimated mortality represents less than 0.01% of the search, leading to an average exposure of 1.5 days. Our their Canadian populations. Avian Conservation and Ecology 8(2): 10 http://www.ace-eco.org/vol8/iss2/art10/

Nevertheless, mortality effects could be potentially important bird populations, through lost productivity, the effects of for individual species over the long-term, e.g., 10 - 20 years, which are equivalent to nest mortality, are lower than that of especially if wind farms are poorly sited. For example, at a direct mortality. At the provincial level, effects of direct habitat wind farm on Smola Island, Norway, prior to construction, loss from wind turbines may be more pronounced in less approximately 13 White-tailed Eagle (Haliaeetus albicilla) common habitat types, e.g., mixed forest in Prince Edward pairs occupied territories within 500 m of the proposed site, Island. However, our overall estimates of nesting habitat loss whereas in 2009 only five pairs occupied territories (Nygard are still much smaller than habitat loss due to many other forms et al. 2010). Between 2005 and 2009, 36 White-tailed Eagles of development such as forestry, agriculture, and mining (see were killed on the Smola Island suggesting that these collisions Calvert et al. 2013). were directly impacting the local population of eagles. Some In addition to the direct loss of habitat, birds may avoid concerns have been expressed that wind turbines in North foraging, nesting, and roosting habitats near wind farms during America could have negative impacts on long-lived species construction activities and operation, thus effectively with low reproductive rates such as Golden Eagles (Aquila decreasing habitat quality beyond the immediate footprint of chrysaetos; see Hunt et al. 1998) though population level the turbine (Band et al. 2007, Higgins et al. 2007). The quantitative data to support this concern have not been importance of this indirect effect has rarely been measured, published. Mortality for species at risk is a particular concern but varies among species depending on their life history, because any incremental mortality could potentially slow behavior, and habitat requirements (Desholm 2009). For recovery. However, even for Chimney Swifts (Chaetura example, some species of birds breeding near wind farms pelagica), a species that is threatened nationally, wind turbine habituate to the presence and operation of the turbines over related mortality only affects 0.03% of the population. time, e.g., Pink-footed Goose (Anser brachyrhynchus; Madsen Nevertheless, as the number of turbines increases, and given and Boertmann 2008), while others tend to avoid these areas that many Canadian birds also migrate through the United because turbines obstruct flight paths and feeding areas States where they are exposed to many more turbines, (Pearce-Higgins et al. 2009). Some grassland breeding birds, population effects may eventually become an issue for some for example, avoid nesting within 100 - 200 m of turbines, species if they are particularly vulnerable to turbines. although at the Ponnequin Wind Energy Facility in Colorado, Loss of nesting habitat and nest mortality estimates grassland songbirds, e.g., Horned Larks and Western The other potential source of wind farm-related bird mortality Meadowlarks (Sturnella neglecta), forage directly beneath is the destruction of nests during construction. Nest mortality turbines (cited in Kerlinger and Dowdell 2003). At the might occur if vegetation containing nests is cleared or Simpson Ridge Wind Farm in Wyoming, female survival, nest destroyed during the bird breeding season. If all construction success, and brood survival were not statistically different in was conducted during the breeding season, based on nest areas with and without turbines, although the authors caution density estimates, approximately 5700 nests would have been that long-term data from multiple locations are needed to destroyed. However, limited available evidence from validate their results (Johnson et al. 2012). Insufficient data postconstruction monitoring reports suggests that most were available in postconstruction monitoring reports used in construction activities occur outside of the breeding bird this study to assess the effect of avoidance of foraging, nesting, season. For example, in Ontario, we estimated that only 20% or roosting habitats on birds in Canada. of projects conduct clearing activities during the breeding Conservation implications season. In the prairies, up to 50% of projects may carry out The accuracy of collision mortality estimates depends strongly some vegetation clearing during the breeding season, with the on the reliability of correction factors used to account for potential to induce nest mortality. The number of nests incomplete carcass detections. Environment Canada’s wind disturbed or destroyed from construction activities can be energy guidelines (Environment Canada 2007a,b) provides minimized if construction activities are conducted outside of guidance on the assessment of potential impacts of wind the breeding season. energy projects on migratory birds in Canada and the type of In addition to collision and nest mortality, birds may also be correction factors that need to be considered during impacted by the loss of nesting habitat as a result of postconstruction monitoring studies. However, specific data construction activities that remove vegetation for the turbine collection protocols were not included in these guidelines to pads and infrastructure, i.e., electrical lines, substation, access accommodate the diversity of landscape and habitat types that roads. According to our estimates, approximately 1.23 ha of exist across Canada. Given concerns about the uncertainty and vegetation is removed per turbine, resulting in a loss of biases associated with correction factors, national standards approximately 3600 ha; an area equivalent to 500 km of a should be established to ensure that correction factors are typical four-lane highway, including shoulders and ditches. robust and defensible and that the estimated impacts of wind Assuming nearby habitats are saturated, and two adults energy developments on migratory birds are accurate. Further displaced per nest site, effects of direct habitat loss on reducing directed research on the expected carcass distribution in Avian Conservation and Ecology 8(2): 10 http://www.ace-eco.org/vol8/iss2/art10/

relation to distance from turbines would reduce uncertainty associated with this correction factor. Acknowledgments: Overall, based on the assumptions and limitation outlined in We would like to thank Natural Resources Canada for this study, the combined effects of collisions, nest mortality, providing many of the postconstruction monitoring reports to and lost habitat on birds associated with Canadian wind farms the authors. We are grateful to those wind developers that also appear to be relatively small compared to other sources of provided data for this manuscript. Tom Levy provided helpful mortality. Although total mortality is anticipated to increase comments on early drafts of the analyses. We would also like substantially as the number of turbines increases, even a to thank Mike Anissimoff who provided assistance in compiling tenfold increase would represent mortality orders of these data and Craig Machtans for providing leadership and magnitude smaller than from many other sources of collision funding from Environment Canada for this project. Finally, mortality in Canada (Calvert et al. 2013). Habitat loss is also we would like to thank two anonymous reviewers for providing relatively small compared to many other forms of constructive and thoughtful comments on this manuscript. development, including road development. Population level impacts are unlikely on most species of birds, provided that highly sensitive or rare habitats, as well as concentration areas LITERATURE CITED for species at risk, are avoided. Arnold, T. W., and R. M. Zink. 2011. Collision mortality has no discernible effect on population trends of North American Although, at a national level, mortality associated with wind birds. PLos One 6(9):e24708. http://dx.doi.org/10.1371/ energy developments in Canada is unlikely to affect most bird journal.pone.0024708 populations based on the approach used in our study, this may not be true for other wildlife such as bats. For example, at Atienza, J. C., I. M. Fierro, O. Infante, J. Valls, and J. some wind farms in Canada, the estimated mortality rate is > Dominguez. 2011. Directrices para la evaluacion del impacto 45 bats per turbine annually. It is uncertain whether this level de los parques eolicos en aves y murcielagos (version 3.0). of mortality could have population level impacts because no SEO/Birdlife, Madrid, Spain. reliable estimates are currently available of population sizes Band, W., M. Madders, and D. P. Whitfield. 2007. Developing for most species. 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